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. 2020 May;14(5):1304-1315.
doi: 10.1038/s41396-020-0604-8. Epub 2020 Feb 14.

Double-stranded DNA virioplankton dynamics and reproductive strategies in the oligotrophic open ocean water column

Elaine Luo  1 , John M Eppley  1 , Anna E Romano  1 , Daniel R Mende  1 , Edward F DeLong  2
Affiliations

Double-stranded DNA virioplankton dynamics and reproductive strategies in the oligotrophic open ocean water column

Elaine Luo et al. ISME J. 2020 May.

Abstract

Microbial communities are critical to ecosystem dynamics and biogeochemical cycling in the open oceans. Viruses are essential elements of these communities, influencing the productivity, diversity, and evolution of cellular hosts. To further explore the natural history and ecology of open-ocean viruses, we surveyed the spatiotemporal dynamics of double-stranded DNA (dsDNA) viruses in both virioplankton and bacterioplankton size fractions in the North Pacific Subtropical Gyre, one of the largest biomes on the planet. Assembly and clustering of viral genomes revealed a peak in virioplankton diversity at the base of the euphotic zone, where virus populations and host species richness both reached their maxima. Simultaneous characterization of both extracellular and intracellular viruses suggested depth-specific reproductive strategies. In particular, analyses indicated elevated lytic interactions in the mixed layer, more temporally variable temperate phage interactions at the base of the euphotic zone, and increased lysogeny in the mesopelagic ocean. Furthermore, the depth variability of auxiliary metabolic genes suggested habitat-specific strategies for viral influence on light-energy, nitrogen, and phosphorus acquisition during host infection. Most virus populations were temporally persistent over several years in this environment at the 95% nucleic acid identity level. In total, our analyses revealed variable distributional patterns and diverse reproductive and metabolic strategies of virus populations in the open-ocean water column.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1. Depth profiles of time-averaged viral and prokaryotic contributions to total sequenced DNA
in a virus-enriched and b cell-enriched size fractions. Relative abundances of viral populations are colored by average amino acid identity (AAI) (>60% AAI across >50% genes) to known phages in RefSeq, and five other viral metagenomic datasets: uvMED [50], uvDEEP [23], Med2017 [24], GOV [15], and EV [16]. Legend shows number of populations identified in each category.
Fig. 2
Fig. 2. α-diversity depth profiles of viral and prokaryotic assemblages:
a Shannon diversity, b richness (number of populations), and c evenness (Shannon diversity divided by log richness). Solid and open circles represent viral and prokaryotic assemblages, respectively, averaged through time (mean ± SE).
Fig. 3
Fig. 3. Spatiotemporal distributions of annotated virus populations present in the virus-enriched size fraction.
Each node on the top dendrogram and its associated column represents the coverage profile of one virus population, colored by its corresponding taxonomic annotation. Rows represent individual samples that are horizontally ordered by depth and time. The height of the black bar in every sample shows mean interquartile range (IQR) coverage of every population, normalized to the maximum IQR coverage in that sample. Time-averaged depth profiles (mean ± SE) of environmental variables of photosynthetically active radiation (PAR), fluorometric chlorophyll a, and inorganic nitrogen are shown in colored triangles on the right panel (data retrieved from Hawaii Ocean Time-Series HOT-DOGS application).
Fig. 4
Fig. 4. Depth profiles of relative abundances of putative temperate phages.
Circles represent time-averaged depth profiles (mean ± SE) of the proportion of all viruses that were identified as temperate in the virus-enriched size fraction (closed circles) and cell-enriched size fraction (open circles).
Fig. 5
Fig. 5. Depth profiles of temporal variabilities of VC ratios (mean ± SE) of 1352 inferred temperate phages (blue) and other viral populations (orange).
Higher VC ratio temporal variability indicates episodic production of free viral particles, while lower variability indicates consistent production of free viral particles. Temporal variability of VC ratios is calculated for each population by pooling its VC ratios within each depth to determine the mean-normalized variance.
Fig. 6
Fig. 6. Distribution of viruses containing specific auxiliary metabolic genes (AMGs) in the water column.
Solid circles show depth profiles, averaged through time (mean ± SE), of the abundance-normalized proportion of virus populations carrying auxiliary metabolic genes respectively for carbon, nitrogen, and phosphorus metabolism: a photosystem, b ammonium transporter, and c phoH. Time-averaged depth profiles of the following are included for environmental context: a relative abundances of cyanophages in the virus-enriched fraction (small open circles) and of cyanobacteria in the cell-enriched fraction (large open circles), photosynthetically active radiation (PAR) (yellow triangles), and fluorometric chlorophyll a (green triangles); b Thaumarchaeal relative abundance in the cell-enriched fraction (open circles) and inorganic nitrogen concentrations (purple triangles). c. total dissolved nitrogen (blue triangles), phosphorus (red triangles), and their ratio (open circles). Environmental metadata were retrieved from Hawaii Ocean Time-Series HOT-DOGs application. Gray box highlights depths around the deep chlorophyll maximum (DCM).
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